Function of the appendages in tentacled snakes (Erpeton tentaculatus).

We investigated the function of the tentacles in aquatic, piscivorous tentacled snakes (Erpeton tentaculatus) by examining anatomy, peripheral innervation, and the response properties of primary afferents. We also investigated visual and somatosensory responses in the optic tectum and documented predatory strikes to visual stimuli and under infrared illumination. Our results show the tentacles are sensitive mechanoreceptors that respond to water movements. They are innervated by rami of the maxillary and ophthalmic branches of the trigeminal nerve and contain a dense array of fine terminal neurites that cross the interior of the tentacle orthogonal to its long axis. The optic tectum contained a retinotopic map of contralateral receptive fields with superior fields represented dorsally in the tectum, inferior fields represented laterally, nasal fields represented rostrally, and temporal fields represented caudally. Large somatosensory receptive fields were identified in deeper layers of the tectum and were in approximate register with overlying visual fields. Tentacled snakes struck accurately at a simulated digital fish, indicating that visual cues are sufficient to guide strikes, but they also captured fish under infrared illumination, suggesting water movements alone could be used to localize prey. We conclude the tentacles are mechanosensors that are used to detect fish position based on water movements and that visual and mechanosensory cues may be integrated in the tectum to enhance localization when visual cues are reduced.

Variation in ovarian morphology in four species of New World moles with a peniform clitoris.

Female moles of the Old World genus Talpa display a curious suite of reproductive features that include a peniform clitoris and ovaries with a discrete interstitial gland or testis-like region (so-called 'ovotestes'). The masculinization of the female external genitalia in Talpa has accordingly been linked with secretion of androgens from the interstitial gland region of the fetal gonad. Although their ovarian morphology has received less attention, some species of New World moles also have ovaries with a pronounced interstitial gland (for example star-nosed mole, Condylura cristata), whereas females of other species do not (for example eastern mole, Scalopus aquaticus). Although it is difficult to determine the sex of both Old and New World moles, published accounts describing the external genitalia of female moles are available only for Talpa. The hypothesis that masculinization of the female external genitalia in moles is associated with the presence of an ovarian interstitial gland (OIG) was tested in the present study by using a comparative approach to determine whether these features are ever found in isolation of one another. Three genera of North American moles (Scapanus, Condylura and Neurotrichus) were studied and a peniform clitoris was found in all three species, but OIG were found in only two of three genera. The ovaries of S. latimanus and S. orarius were unremarkable, with no evidence of a discrete interstitial gland or testis-like region. Mapping these results onto recent talpid phylogenies indicates that loss of the bipolar ovarian morphology is a derived trait in Scapanus, and conclusively demonstrates that masculinization of the external genitalia in female moles can develop in the presence or absence of 'ovotestes'.

Effects of stimulus duration on neuronal response properties in the somatosensory cortex of the star-nosed mole.

Star-nosed moles have a series of mechanosensory appendages surrounding each nostril. Each appendage is covered with sensory organs (Eimer's organs) containing both rapidly adapting and slowly adapting mechanoreceptors and each appendage is represented in primary somatosensory cortex (S1) by a single cortical module. When the skin surface of an appendage is depressed, neurons in the corresponding module in S1 respond in either a transient or sustained fashion. The aim of this study was to characterize and compare the responses of these two classes of neurons to both short (5 or 20 ms) and long (500 ms) mechanosensory stimulation. Activity from neurons in the representation of appendage 11, the somatosensory fovea, was recorded while delivering mechanosensory stimuli to the corresponding skin surface. Transient and sustained neurons had different levels of spontaneous activity and different responses to both short and long mechanosensory stimulation. Neurons with sustained responses had a significantly higher spontaneous firing rate than neurons with transient responses. Transient neurons responded to a 5 ms stimulus with excitation followed by suppression of discharge whereas sustained neurons did not exhibit post-excitatory suppression. Rather, responses of sustained neurons to 5 ms stimuli lasted several hundred milliseconds. Consequently sustained responses contained significantly more spikes than transient responses. These experiments suggest contact to the appendages causes two distinct firing patterns in cortex regardless of the duration of the stimulus. The sustained and transient responses could reflect either the activity of fundamentally different classes of neurons or activity in distinct subcortical and cortical networks.

Early development of a somatosensory fovea: a head start in the cortical space race?

Star-nosed moles have 11 mechanosensory appendages surrounding each nostril, and primary afferents from a single appendage-the tactile fovea-are greatly over-represented in somatosensory cortex. It was found that the foveal appendage led development in the periphery, had the greatest innervated surface area in embryos, and developed mature nerve terminals and epidermal sensory organs first; also, in developing cortex, markers for metabolic activity (cytochrome oxidase) appeared first in the fovea representation. This developmental sequence may provide the fovea with an advantage in a competition for cortical space, and account for the much larger areas of cortex devoted to foveal afferents.

Anatomic correlates of the face and oral cavity representations in the somatosensory cortical area 3b of monkeys.

We determined the somatotopy of the face and the oral cavity representation in cortical area 3b of New World owl monkeys and squirrel monkeys. Area 3b is apparent as a densely myelinated strip in brain sections cut parallel to the surface of flattened cortex. A narrow myelin-light septum that we have termed the "hand-face septum" separates the hand representation from the more lateral face and mouth representation. The face and oral cavity representation is further divided into a series of myelin-dense ovals. We show that three ovals adjacent to the hand representation correspond to the upper face, upper lip, and chin plus lower lip, whereas three or four more rostral ovals successively represent the contralateral teeth, tongue, and the ipsilateral teeth and tongue. Strips of cortex lateral and medial to the area 3b ovals, possibly corresponding to area 1 and area 3a, respectively, have similar somatotopic sequences. Although previous results suggest the existence of great variability within and across primate species, we conclude that the representations of the face and mouth are highly similar across individuals of the same species, and there are extensive overall similarities across these two species of New World monkeys.

Areal and callosal connections in the somatosensory cortex of the star-nosed mole.

Star-nosed moles have a well-developed somatosensory cortex with multiple cortical areas representing the behaviorally important tactile star. In each of three cortical representations, the 11 mechanosensory appendages from the contralateral nose are represented in a series of dark cytochrome oxidase modules. Here the connections of this complex cortical network were explored with injections of the neuroanatomical tracer wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). The main goal was to determine the connection patterns of the somatosensory areas that represent the star. Injections of tracer made in or around the primary somatosensory representation (S1) of the star allowed us to determine the topography of local cortical connections and the projection and termination sites of corresponding interhemispheric connections. The results revealed precise topographic corticocortical connections reciprocally interconnecting the S1 star representation with its counterparts in S2 and in a third representation (S3) unique to star-nosed moles. Callosal connections from a widespread area of the contralateral hemisphere terminated primarily in the septa between cytochrome oxidase dark modules and in areas of cortex surrounding the star representations. However, midline structures of the star represented in S1 and S2 exhibited a high level of callosally labeled cells and terminals. This included label both within septa and within the centers of cytochrome oxidase dense modules representing midline appendages.

Distribution and innervation of taste buds in the axolotl.

Adult axolotls have approximately 1,400 taste buds in the epithelium of the pharyngeal roof and floor and the medial surfaces of the visceral bars. These receptors are most dense on the lingual surfaces of the upper and lower jaws, slightly less dense throughout lateral portions of the pharyngeal roof and floor, and more sparse within medial portions of the pharyngeal roof and floor, except for a median oval patch of receptors located rostrally between the vomerine tooth fields. Each taste bud is a pear-shaped organ, situated at the center of a raised hillock and averaging 80 and 87 microm in height and width, respectively. Each comprises 50 to 80 cells, which can be classified as basal, dark fusiform, or light fusiform, based on differences in their morphology. The distal ends of the apical processes of the fusiform cells reach the surface of each hillock, forming a single taste pore with an average diameter of 15 microm. Each apical process terminates in one of three ways: as short, evenly spaced microvilli; as long clustered microvilli; or as large, stereocilia-like microvilli. The pharyngeal epithelium and associated taste buds in axolotls are innervated solely by rami of the facial, glossopharyngeal and vagal nerves. Approximately, the rostral one half of the pharyngeal roof is innervated by the palatine rami of the facial nerve, whereas the caudal one half of the pharyngeal roof is innervated by the pharyngeal rami of the glossopharyngeal and vagal nerves. The lingual surface of the lower jaw is innervated by the pretrematic (mandibular) ramus of the facial nerve. The dorsal two-thirds of the visceral arches, and the ventral one-third of the visceral arches and the pharyngeal floor, are innervated by both the pretrematic and post-trematic rami of the glossopharyngeal and vagal nerves, respectively.

Epidermal sensory organs of moles, shrew moles, and desmans: a study of the family talpidae with comments on the function and evolution of Eimer's organ.

The epidermal sensory organs of members of the family Talpidae (moles, shrew-moles, and desmans) were investigated and compared to determine the range of sensory specializations and better understand how they evolved. Small domed mechanosensory organs called 'Eimer's organs' were present on the rhinarium of nearly all species of talpids, but not among the sister group of shrews (Soricidae) or other insectivore families. This suggests that the common ancestor to the talpids possessed Eimer's organs. Two species of moles from the driest habitats did not exhibit Eimer's organs - suggesting that their sensory organs degenerated in response to harsh, abrasive soil conditions. The semi-aquatic desmans uniquely possessed tiny sensory hairs interspersed with their Eimer's organs; these may act to sense water currents. Some species exhibited a subdivided, star-like, rhinarium - resembling an early embryonic stage of the star-nosed mole and providing clues to the evolution of the star. A single genera (Uropsilus) that branched off early in the evolution of the talpids had Eimer's organ-like structures but lacked some typical components. These findings fill a major gap in our knowledge of talpid sensory biology and suggest (1) how Eimer's organs evolved, (2) how the unusual appendages of the star-nosed mole evolved, (3) that the evolution of Eimer's organ is convergent with the mechanosensory push-rod of monotremes. The results also demonstrate the features that distinguish Eimer's organ from similar configurations of sensory receptors in other mammalian skin surfaces. Finally, a mechanism for Eimer's organ function in detecting object and prey specific surface features is proposed.

Cortical-organization in moles: evidence of new areas and a specialized S2.

The somatosensory cortex of several mole species (family Talpidae), with different peripheral sensory adaptations, was investigated and compared to determine common and specialized features of cortical organization. Previously unidentified medial representations of the trunk and limbs were found in all species, indicating that S1 in moles occupies a medial to lateral strip of cortex as in most other mammals. This finding suggests a large lateral forelimb representation, previously attributed to S1, is actually part of S2. In the face representation, evidence was found for three representations of the unusual nose of the star-nosed mole (Condylura cristata). Each of these areas was divided into a series of modules (visible in cytochrome oxidase processed tissue) representing individual nasal appendages on the star. In the closely related but less specialized eastern mole (Scalopus aquaticus) and coast mole (Scapanus orarius), only two nose representations were identified in an area of cortex with a more uniform histological appearance. The results indicate that moles have enlarged somatosensory representations of the glabrous nose as compared to shrews and rats that instead have large vibrissal representations. In addition moles have a very large and specialized representation of the digging forepaw in S2. Since this part of S2 projects directly to the cervical spinal cord, the specialization may provide adaptive sensorimotor functions related to digging.

Cortical organization in insectivora: the parallel evolution of the sensory periphery and the brain.

Insectivores are traditionally described as a primitive group that has not changed much in the course of mammalian evolution. In contrast, recent studies reveal a great diversity of sensorimotor specializations among insectivores adapted to a number of different ecological niches, indicating that there has been significant diversification and change in the course of their evolution. Here the organization of sensory cortex is compared in the African hedgehog (Atelerix albiventris), the masked shrew (Sorex cinereus), the eastern mole (Scalopus aquaticus), and the star-nosed mole (Condylura cristata). Each of these four closely related species lives in a unique ecological niche, exhibits a different repertoire of behaviors, and has a different configuration of peripheral sensory receptors. Corresponding specializations of cortical sensory areas reveal a number of ways in which the cortex has evolved in parallel with changes to the sensory periphery. These specializations include expansion of cortical representations (cortical magnification), the addition or loss of cortical areas in the processing network, and the subdivision of areas into modules (barrels and stripes).

The organization of somatosensory cortex in the short-tailed opossum (Monodelphis domestica).

The organization of neocortex in the short-tailed opossum (Monodelphis domestica) was explored with multiunit microelectrode recordings from middle layers of cortex. Microelectrode maps were subsequently related to the chemoarchitecture of flattened cortical preparations, sectioned parallel to the cortical surface and processed for either cytochrome oxidase (CO) or NADPH-diaphorase (NADPHd) histochemistry. The recordings revealed the presence of at least two systematic representations of the contralateral body surface located in a continuous strip of cortex running from the rhinal sulcus to the medial wall. The primary somatosensory area (S1) was located medially while secondary somatosensory cortex (S2) formed a laterally located mirror image of S1. Auditory cortex was located in lateral cortex at the caudal border of S2, and some electrode penetrations in this area responded to both auditory and somatosensory stimulation. Auditory cortex was outlined by a dark oval visible in flattened brain sections. A large primary visual cortex (V1) was located at the caudal pole of cortex, and also consistently corresponded to a large chemoarchitecturally visible oval. Cortex just rostral and lateral to V1 responded to visual stimulation, while bimodal auditory/visual responses were obtained in an area between V1 and somatosensory cortex. The results are compared with brain organization in other marsupials and with placentals and the evolution of cortical areas in mammals is discussed.

Organization of sensory cortex in the East African hedgehog (Atelerix albiventris).

We investigated the organization of neocortex in the East African hedgehog (Atelerix albiventris) with microelectrode recordings from sensory areas that were later correlated with cytochrome oxidase patterns in sections of flattened cortex. The location of corticospinal projecting neurons was also examined and related to sensory areas by making small injections of wheat germ agglutinin-horseradish peroxidase into the spinal cord. Our goals were to determine how hedgehog cortex is organized, how much sensory areas overlap, and to compare results with recent findings in other insectivores. Evidence was found for three separate topographically organized somatosensory areas, two visual areas, and a caudolateral auditory area. A medial somatosensory area corresponded to S1, the primary somatosensory area, whereas two lateral areas partially encircled auditory cortex and corresponded to the parietal ventral area (PV) and the secondary somatosensory area (S2). Primary visual cortex (V1) was delineated by a caudomedial cytochrome oxidase dark oval, and a more lateral visual area between V1 and somatosensory cortex corresponded to V2, or area 18. Two patches of corticospinal projecting cells were found primarily overlapping S1 and S2. Some bimodal auditory and somatosensory responses were found in parts of PV and S2, but for the most part, areas had relatively sharp histochemically apparent and physiologically defined borders. The present results indicate that the caudal neocortex of hedgehogs has only a few sensory areas, corresponding to those commonly found in several other small-brained mammals. Hedgehog cortical organization differs significantly in somatotopy, number, and position of fields from that of closely related shrews and moles. Thus, clear specializations occur, even within the order Insectivora.

Distribution of NADPH-diaphorase cells in visual and somatosensory cortex in four mammalian species.

The distribution of the well-labeled nicotinamide adenine dinucleotide phosphate diaphorase (NADPHd) Type I neurons was evaluated in the isocortex of four mammalian species: the Didelphis opossum, the Monodelphis opossum, the rat and the marmoset. In Didelphis opossum, laminar distribution was examined in tangential and non-tangential sections. The density increases from superficial to deep layers of the gray matter. In rats' tangential sections, infragranular and supragranular layers have higher density than layer IV. Cell density measurements in the visual and the somatosensory cortices were compared in tangential sections from flattened hemispheres of the four species. Somatosensory areas were identified histochemically in rat (barrel fields) and marmoset (S1 and S2/PV). In the opossums, areas S1 and S2/PV were identified by multiunit recording. Except in the rat, primary visual cortex (V1) was labeled histochemically by NADPHd and/or cytochrome oxidase. In the four species, cell density in somatosensory cortex was significantly higher than in visual cortex. Taken together these results demonstrate that NADPHd Type I neurons are not homogeneously distributed in the isocortex of these mammals. In conclusion, the tangential distribution of Type I neurons in the sensory areas examined, but not its laminar distribution, was similar in the four species. Given that rats, marmosets and opossums are distantly related species, and that the latter are considered to have more 'generalized' brains, it is conceivable that this pattern of tangential distribution of Type I neurons is a general feature of mammalian isocortex.

A nose that looks like a hand and acts like an eye: the unusual mechanosensory system of the star-nosed mole.

The star-nosed mole (Condylura cristata) has a snout surrounded by 22 fleshy and mobile appendages. This unusual structure is not an olfactory organ, as might be assumed from its location, nor is it used to manipulate objects as might be guessed from its appearance. Rather, the star is devoted to the sense of touch, and for this purpose the appendages are covered with thousands of small mechanoreceptive Eimer's organs. Recent behavioral studies find that the star acts much like a tactile eye, having a small behavioral focus, or "fovea" at the center--used for detailed explorations of objects of interest. The peripheral and central nervous systems of the mole reflect these behavioral specializations, such that the small behavioral focus on the nose is more densely innervated in the periphery, and has a greatly enlarged representation in the somatosensory cortex. This somatosensory representation of the tactile fovea is not correlated with anatomical parameters (innervation density) as found in other species, but rather is highly correlated with patterns of behavior. The many surprising parallels between the somatosensory system of the mole, and the visual systems of other mammals, suggest a convergent and perhaps common organization for highly developed sensory systems.

The development of a biological novelty: a different way to make appendages as revealed in the snout of the star-nosed mole Condylura cristata.

The nose of the star-nosed mole Condylura cristata is a complex biological novelty consisting of 22 epidermal appendages. How did this new set of facial appendages arise? Recent studies find remarkable conservation of the genes expressed during appendage formation across phyla, suggesting that the basic mechanisms for appendage development are ancient. In the nose of these moles, however, we find a unique pattern of appendage morphogenesis, showing that evolution is capable of constructing appendages in different ways. During development, the nasal appendages of the mole begin as a series of waves in the epidermis. A second deep layer of epidermis then grows under these superficial epidermal waves to produce 22 separate, elongated epidermal cylinders embedded in the side of the mole's face. The caudal end of each cylinder later erupts from the face and rotates forward to project rostrally, remaining attached only at the tip of the snout. As a result of this unique 'unfolding' formation, the rostral end of each adult appendage is derived from caudal embryonic facial tissue, while the caudal end of each appendage is derived from rostral facial tissue. This developmental process has essentially no outgrowth phase and results in the reversal of the original embryonic orientation of each appendage. This differs from the development of other known appendages, which originate either as outgrowths of the body wall or from subdivisions of outgrowths (e.g. tetrapod digits). Adults of a different mole species (Scapanus townsendii) exhibit a star-like pattern that resembles an embryonic stage of the star-nosed mole, suggesting that the development of the star recapitulates stages of its evolution.

Cortical organization in shrews: evidence from five species.

Cortical organization was examined in five shrew species. In three species, Blarina brevicauda, Cryptotis parva, and Sorex palustris, microelectrode recordings were made in cortex to determine the organization of sensory areas. Cortical recordings were then related to flattened sections of cortex processed for cytochrome oxidase or myelin to reveal architectural borders. An additional two species (Sorex cinereus and Sorex longirostris) with visible cortical subdivisions based on histology alone were analyzed without electrophysiological mapping. A single basic plan of cortical organization was found in shrews, consisting of a few clearly defined sensory areas located caudally in cortex. Two somatosensory areas contained complete representations of the contralateral body, corresponding to primary somatosensory cortex (S1) and secondary somatosensory cortex (S2). A small primary visual cortex (V1) was located closely adjacent to S1, whereas auditory cortex (A1) was located in extreme caudolateral cortex, partially encircled by S2. Areas did not overlap and had sharp, histochemically apparent and electrophysiologically defined borders. The adjacency of these areas suggests a complete absence of intervening higher level or association areas. Based on a previous study of corticospinal connections, a presumptive primary motor cortex (M1) was identified directly rostral to S1. Apparently, in shrews, the solution to having extremely little neocortex is to have only a few small cortical subdivisions. However, the small areas remain discrete, well organized, and functional. This cortical organization in shrews is likely a derived condition, because a wide range of extant mammals have a greater number of cortical subdivisions.

A histologically visible representation of the fingers and palm in primate area 3b and its immutability following long-term deafferentations.

An isomorph of the glabrous hand is visible in primary somato-sensory cortex (area 3b) of owl monkeys in brain sections cut parallel to the surface and stained for myelin. A mediolateral row of five ovals, separated by myelin-light septa, represents digits and corresponds precisely with cortical sites activated by light touch on individual digits in microelectrode recordings. A number of caudal ovals relate to pads of the palm. A more distinct septum separates the hand from the more lateral face representation. Within the face representation, two large myelin-dense ovals can be identified that are activated by the upper or lower face in a caudo-rostral sequence. Accidental finger loss or dorsal column section, deafferentations that result in reorganization of the physiological map in area 3b, do not alter the morphological map. The proportions for each digit and palm in the morphological map do not vary across normal and deafferented animals. Similar isomorphs were also seen in area 3b of squirrel and macaque monkeys. We conclude that the anatomical isomorph for the body surface representation in area 3b is a reliable reflection of normal cortical organization and may be a common feature of the primate area 3b. The isomorph can provide a reference in studies of somatotopic reorganization.

Somatosensory fovea in the star-nosed mole: behavioral use of the star in relation to innervation patterns and cortical representation.

Eleven fleshy appendages, or rays, surround each of the nostrils of the star-nosed mole. Each ray is covered with tactile sensory organs, and each ray is represented in the cortex by a stripe of tissue visible in brain sections processed for cytochrome oxidase. Here we report that the 11th, ventral ray is the behavioral focus of the nose. This ray is preferentially used to explore prey items by touch, in a behavior pattern similar to the use of a fovea in the visual system. After prey is first contacted with any nasal ray, subsequent touches are centered on the 11th ray. Although the 11th ray is small and has relatively few sensory organs on its surface, it has the largest cortical representation, greatest area of cortex per sensory organ, and the highest innervation density per sensory organ. In addition, the average area of cortex per primary afferent is highest for this ray. We refer to the differential magnification of first-order afferents in the cortical representation as "afferent magnification." The patterns of both cortical magnification (cortical area per sensory organ) and afferent magnification (cortical area per afferent) of the rays correlated highly with the distribution of touches across the nose scored from videotaped behavior. A simple model of star-nosed mole behavior predicts the distribution of touches across the rays and also correlates highly with both the actual pattern of behavior and the patterns of cortical magnification observed.

Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury.

Sensory stimuli to the body are conveyed by the spinal cord to the primary somatosensory cortex. It has long been thought that dorsal column afferents of the spinal cord represent the main pathway for these signals, but the physiological and behavioural consequences of cutting the dorsal column have been reported to range from mild and transitory to marked. We have re-examined this issue by sectioning the dorsal columns in the cervical region and recording the responses to hand stimulation in the contralateral primary somatosensory cortex (area 3b). Following a complete section of the dorsal columns, neurons in area 3b become immediately and perhaps permanently unresponsive to hand stimulation. Following a partial section, the remaining dorsal column afferents continue to activate neurons within their normal cortical target territories, but after five or more weeks the area of activation is greatly expanded. After prolonged recovery periods of six months or more, the deprived hand territory becomes responsive to inputs from the face (which are unaffected by spinal cord section). Thus, area 3b of somatosensory cortex is highly dependent on dorsal spinal column inputs, and other spinal pathways do not substitute for the dorsal columns even after injury.

Organization of somatosensory cortex and distribution of corticospinal neurons in the eastern mole (Scalopus aquaticus).

The somatotopic organization of somatosensory cortex of the eastern mole (Scalopus aquaticus) was explored with multiunit microelectrode recordings from middle layers of cortex. The recordings revealed the presence of at least parts of two systematic representations of the body surface in the lateral cortex. One of the representations appears to be primary somatosensory cortex (S1), and it contained cytochrome oxidase dark regions, separated by light septa that formed isomorphs with some body parts. The rostral portion of this presumptive S1 cortex contained a face representation with a series of barrel-like cytochrome oxidase dark ovals that corresponded to the vibrissae on the snout. In caudolateral S1, light septa outline the palm and digits of the forepaw. Cortex caudal to S1, in the expected region of auditory cortex, responded to vibration, suggesting a modification of auditory cortex. Injections of wheat germ agglutinin-horseradish peroxidase into the cervical enlargement of the spinal cord revealed two dense foci of cortical cells that project to the spinal cord. The focus medial to the face region in S1 may correspond to primary motor cortex (M1). The second focus was coextensive with the somatosensory representation of the forelimb and the trunk in S1. The dense corticospinal projections from the forelimb representation of S1 and motor cortex may reflect sensorimotor specializations related to digging behaviors in moles.